Complete genome sequences and comparative secretomic analysis for the industrially cultivated edible mushroom Lyophyllum decastes reveals insights on evolution and lignocellulose degradation potential

Lyophyllum decastes, also known as Luronggu in China, is a culinary edible and medicinal mushroom that was widely cultivated in China in recent years. In the present study, the complete high-quality genome of two mating compatible L. decastes strain was sequenced. The L. decastes LRG-d1-1 genome con...

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Main Authors: Lili Xu, Wujie Yang, Tianmei Qiu, Xia Gao, Hongyong Zhang, Shuliang Zhang, Hui Cui, Lizhong Guo, Hailong Yu, Hao Yu
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-03-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2023.1137162/full
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author Lili Xu
Lili Xu
Wujie Yang
Tianmei Qiu
Xia Gao
Hongyong Zhang
Shuliang Zhang
Hui Cui
Lizhong Guo
Hailong Yu
Hao Yu
author_facet Lili Xu
Lili Xu
Wujie Yang
Tianmei Qiu
Xia Gao
Hongyong Zhang
Shuliang Zhang
Hui Cui
Lizhong Guo
Hailong Yu
Hao Yu
author_sort Lili Xu
collection DOAJ
description Lyophyllum decastes, also known as Luronggu in China, is a culinary edible and medicinal mushroom that was widely cultivated in China in recent years. In the present study, the complete high-quality genome of two mating compatible L. decastes strain was sequenced. The L. decastes LRG-d1-1 genome consists of 47.7 Mb in 15 contigs with a contig N90 of 2.08 Mb and 14,499 predicted gene models. Phylogenetic analysis revealed that L. decastes exhibits a close evolutionary relationship to the Termitomyces and Hypsizygus genus and was diverged from H. marmoreus  ~ 45.53 Mya ago. Mating A loci of L. decastes compose of five and four HD genes in two monokaryotic strains, respectively. Mating B loci compose of five STE genes in both two monokaryotic strains. To accelerate the cross-breeding process, we designed four pairs of specific primers and successfully detected both mating types in L. decastes. As a wood-rotting mushroom, a total of 541 genes accounting for 577 CAZymes were identified in the genome of L. decastes. Proteomic analysis revealed that 1,071 proteins including 182 CAZymes and 258 secreted enzymes were identified from four groups (PDB, PDB + bran, PDB + cotton hull, and PDB + sawdust). Two laccases and a quinone reductase were strongly overproduced in lignin-rich cultures, and the laccases were among the top-3 secreted proteins, suggesting an important role in the synergistic decomposition of lignin. These results revealed the robustness of the lignocellulose degradation capacity of L. decastes. This is the first study to provide insights into the evolution and lignocellulose degradation of L. decastes.
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spelling doaj.art-906f850871ed4a78b5436acd65ac52d22023-03-23T16:20:25ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-03-011410.3389/fmicb.2023.11371621137162Complete genome sequences and comparative secretomic analysis for the industrially cultivated edible mushroom Lyophyllum decastes reveals insights on evolution and lignocellulose degradation potentialLili Xu0Lili Xu1Wujie Yang2Tianmei Qiu3Xia Gao4Hongyong Zhang5Shuliang Zhang6Hui Cui7Lizhong Guo8Hailong Yu9Hao Yu10Shandong Provincial Key Laboratory of Applied Mycology, School of Life Sciences, Qingdao Agricultural University, Qingdao, Shandong, ChinaNational Engineering Research Center of Edible Fungi, Institute of Edible Fungi, Shanghai Academy of Agricultural Sciences, Shanghai, ChinaShandong Agricultural Technology Extending Station, Jinan, Shandong, ChinaShandong Provincial Key Laboratory of Applied Mycology, School of Life Sciences, Qingdao Agricultural University, Qingdao, Shandong, ChinaShandong Agricultural Technology Extending Station, Jinan, Shandong, ChinaDezhou Academy of Agricultural Sciences, Dezhou, Shandong, ChinaDezhou Academy of Agricultural Sciences, Dezhou, Shandong, ChinaShandong Agricultural Technology Extending Station, Jinan, Shandong, ChinaShandong Provincial Key Laboratory of Applied Mycology, School of Life Sciences, Qingdao Agricultural University, Qingdao, Shandong, ChinaNational Engineering Research Center of Edible Fungi, Institute of Edible Fungi, Shanghai Academy of Agricultural Sciences, Shanghai, ChinaShandong Provincial Key Laboratory of Applied Mycology, School of Life Sciences, Qingdao Agricultural University, Qingdao, Shandong, ChinaLyophyllum decastes, also known as Luronggu in China, is a culinary edible and medicinal mushroom that was widely cultivated in China in recent years. In the present study, the complete high-quality genome of two mating compatible L. decastes strain was sequenced. The L. decastes LRG-d1-1 genome consists of 47.7 Mb in 15 contigs with a contig N90 of 2.08 Mb and 14,499 predicted gene models. Phylogenetic analysis revealed that L. decastes exhibits a close evolutionary relationship to the Termitomyces and Hypsizygus genus and was diverged from H. marmoreus  ~ 45.53 Mya ago. Mating A loci of L. decastes compose of five and four HD genes in two monokaryotic strains, respectively. Mating B loci compose of five STE genes in both two monokaryotic strains. To accelerate the cross-breeding process, we designed four pairs of specific primers and successfully detected both mating types in L. decastes. As a wood-rotting mushroom, a total of 541 genes accounting for 577 CAZymes were identified in the genome of L. decastes. Proteomic analysis revealed that 1,071 proteins including 182 CAZymes and 258 secreted enzymes were identified from four groups (PDB, PDB + bran, PDB + cotton hull, and PDB + sawdust). Two laccases and a quinone reductase were strongly overproduced in lignin-rich cultures, and the laccases were among the top-3 secreted proteins, suggesting an important role in the synergistic decomposition of lignin. These results revealed the robustness of the lignocellulose degradation capacity of L. decastes. This is the first study to provide insights into the evolution and lignocellulose degradation of L. decastes.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1137162/fulledible mushroomLyophyllum decastesgenomeproteomesecretomeCAZymes
spellingShingle Lili Xu
Lili Xu
Wujie Yang
Tianmei Qiu
Xia Gao
Hongyong Zhang
Shuliang Zhang
Hui Cui
Lizhong Guo
Hailong Yu
Hao Yu
Complete genome sequences and comparative secretomic analysis for the industrially cultivated edible mushroom Lyophyllum decastes reveals insights on evolution and lignocellulose degradation potential
Frontiers in Microbiology
edible mushroom
Lyophyllum decastes
genome
proteome
secretome
CAZymes
title Complete genome sequences and comparative secretomic analysis for the industrially cultivated edible mushroom Lyophyllum decastes reveals insights on evolution and lignocellulose degradation potential
title_full Complete genome sequences and comparative secretomic analysis for the industrially cultivated edible mushroom Lyophyllum decastes reveals insights on evolution and lignocellulose degradation potential
title_fullStr Complete genome sequences and comparative secretomic analysis for the industrially cultivated edible mushroom Lyophyllum decastes reveals insights on evolution and lignocellulose degradation potential
title_full_unstemmed Complete genome sequences and comparative secretomic analysis for the industrially cultivated edible mushroom Lyophyllum decastes reveals insights on evolution and lignocellulose degradation potential
title_short Complete genome sequences and comparative secretomic analysis for the industrially cultivated edible mushroom Lyophyllum decastes reveals insights on evolution and lignocellulose degradation potential
title_sort complete genome sequences and comparative secretomic analysis for the industrially cultivated edible mushroom lyophyllum decastes reveals insights on evolution and lignocellulose degradation potential
topic edible mushroom
Lyophyllum decastes
genome
proteome
secretome
CAZymes
url https://www.frontiersin.org/articles/10.3389/fmicb.2023.1137162/full
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